Flagellar ion channels of sperm: similarities and differences between species

Miller, Melissa R.; Mansell, Steven A.; Meyers, Stuart A.; Lishko, Polina V.

doi:10.1016/j.ceca.2014.10.009

Cited by 107 publications

(88 citation statements)

References 155 publications

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“…Interestingly, although both human and mouse sperm hyperactivate, only human spermatozoa display full 360 rotation along the long axis, whereas mouse sperm alternate between 180 turns (Babcock et al, 2014). CatSper, which is organized in quadrilateral longitudinal nanodomains along the sperm flagellum (Chung et al, 2014, 2017) is also regulated by species-specific cues (Miller et al, 2015). In human sperm, CatSper is activated by both flagellar alkalinity and progesterone (Lishko et al, 2011; Strünker et al, 2011), whereas, in murine sperm, CatSper is only regulated by the former modality (Kirichok et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Asymmetrically Positioned Flagellar Control Units Regulate Human Sperm Rotation

et al. 2018

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SUMMARY Ion channels control sperm navigation within the female reproductive tract and, thus, are critical for their ability to find and fertilize an egg. The flagellar calcium channel CatSper controls sperm hyperactivated motility and is dependent on an alkaline cytoplasmic pH. The latter is accomplished by either proton transporters or, in human sperm, via the voltage-gated proton channel Hv1. To provide concerted regulation, ion channels and their regulatory proteins must be compartmentalized. Here, we describe flagellar regulatory nanodomains comprised of Hv1, CatSper, and its regulatory protein ABHD2. Super-resolution microscopy revealed that Hv1 is distributed asymmetrically within bilateral longitudinal lines and that inhibition of this channel leads to a decrease in sperm rotation along the long axis. We suggest that specific distribution of flagellar nanodomains provides a structural basis for the selective activation of CatSper and subsequent flagellar rotation. The latter, together with hyperactivated motility, enhances the fertility of sperm.

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Section: Introductionmentioning

confidence: 99%

Asymmetrically Positioned Flagellar Control Units Regulate Human Sperm Rotation

et al. 2018

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“…Like many gamete-specific proteins and the other CatSper proteins reported so far (Cai and Clapham, 2008; Chung et al, 2011), mouse and human CatSper ε and ζ show signs of rapid evolutionary change with only 50% and 45% amino acid sequence identity, respectively. In particular, the sequence regions outside TM segments and the pore loop of CatSper proteins are poorly conserved across species, indicating these regions possibly convey species-specific modulation of flagellar motility (Miller et al, 2015). This is illustrated by striking differences in progesterone-elicited I CatSper responses in mouse and human (Lishko et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

CatSperζ regulates the structural continuity of sperm Ca2+ signaling domains and is required for normal fertility

Chung

Miki

Kim

et al. 2017

eLife

141

285

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We report that the Gm7068 (CatSpere) and Tex40 (CatSperz) genes encode novel subunits of a 9-subunit CatSper ion channel complex. Targeted disruption of CatSperz reduces CatSper current and sperm rheotactic efficiency in mice, resulting in severe male subfertility. Normally distributed in linear quadrilateral nanodomains along the flagellum, the complex lacking CatSperζ is disrupted at ~0.8 μm intervals along the flagellum. This disruption renders the proximal flagellum inflexible and alters the 3D flagellar envelope, thus preventing sperm from reorienting against fluid flow in vitro and efficiently migrating in vivo. Ejaculated CatSperz-null sperm cells retrieved from the mated female uterus partially rescue in vitro fertilization (IVF) that failed with epididymal spermatozoa alone. Human CatSperε is quadrilaterally arranged along the flagella, similar to the CatSper complex in mouse sperm. We speculate that the newly identified CatSperζ subunit is a late evolutionary adaptation to maximize fertilization inside the mammalian female reproductive tract.DOI: http://dx.doi.org/10.7554/eLife.23082.001

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“…SLO1 is modulated by Ca 2+ (Magleby 2003), SLO2.1 and SLO2.2 by Na + and Cl À (Yuan et al 2003;Paulais et al 2006), and SLO3 by pH and voltage (Schreiber et al 1998). SLO3 is only present in sperm and localized probably to its flagella (Schreiber et al 1998;Navarro et al 2007;Miller et al 2015). In fact, the lack of SLO3 in male mice causes infertility (Santi et al 2010;Zeng et al 2011) though they exhibit normal testis size, sperm number (Santi et al 2010), and capacitation-associated protein phosphorylation (Escoffier et al 2015).…”

Section: Slo3 Channelsmentioning

confidence: 99%

“…Electrophysiological recordings of SLO3 either heterologously expressed (Xenopus oocytes/CHO cells) or in testicular/ epididymal sperm have allowed its characterization in terms of pH dependence, modulation by the LRRC52 subunit, and the species-specific sensitivity to inhibitors (Martínez-L opez et al 2009;Santi et al 2010;Tang et al 2010;Zeng et al 2011;L opez-González et al 2014;Sánchez-Carranza et al 2015;Wrighton et al 2015;Zeng et al 2015). The contribution of SLO3 to the AR is not clear; one proposal is that its aperture during capacitation, due to a higher concentration of HCO 3 À and alkaline pH in the female tract, increases the driving force for Ca 2+ entry, probably through CatSper or other channels, triggering the subsequent events that lead to the AR (Lishko et al 2011a;Miller et al 2015). Another hypothesis is that once in the female tract, SLO3 activation hyperpolarizes Em, which in turn stimulates a voltage-dependent Na + /H + exchanger, leading to a further pH i rise, activating CatSper, depolarizing sperm, and setting the conditions for AR (Chávez et al 2014).…”

Section: Slo3 Channelsmentioning

confidence: 99%

Role of Ion Channels in the Sperm Acrosome Reaction

Beltrán

Treviño

Mata-Martínez

et al. 2016

Advances in Anatomy, Embryology and Cell Biology

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The acrosome reaction (AR) is a unique exocytotic process where the acrosome, a single membrane-delimited specialized organelle, overlying the nucleus in the sperm head of many species, fuses with the overlying plasma membrane. This reaction, triggered by physiological inducers from the female gamete, its vicinity, or other stimuli, discharges the acrosomal content modifying the plasma membrane, incorporating the inner acrosomal membrane, and exposing it to the extracellular medium. The AR is essential for sperm-egg coat penetration, fusion with the eggs' plasma membrane, and fertilization. As in most exocytotic processes Ca(2+) is crucial for the AR, as well as intracellular pH and membrane potential changes. Thus, among the required processes needed for this reaction, ion permeability changes involving channels are pivotal. In spite of the key role ion channels play in the AR, their identity and regulation is not fully understood. Though molecular and pharmacological evidence indicates that various ionic channels participate during the AR, such as store-operated Ca(2+) channels and voltage-dependent Ca(2+) channels, whole cell patch clamp recordings have failed to detect some of them until now. Since sperm display a very high resistance and a minute cytoplasmic volume, very few channels are needed to achieve large membrane potential and concentration changes. Functional detection of few channels in the morphologically complex and tiny sperm poses technical problems, especially when their conductance is very small, as in the case of SOCs. Single channel recordings and novel fluorescence microscopy strategies will help to define the participation of ionic channels in the intertwined signaling network that orchestrates the AR.

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Flagellar ion channels of sperm: similarities and differences between species

Cited by 107 publications

References 155 publications

Asymmetrically Positioned Flagellar Control Units Regulate Human Sperm Rotation

Asymmetrically Positioned Flagellar Control Units Regulate Human Sperm Rotation

CatSperζ regulates the structural continuity of sperm Ca2+ signaling domains and is required for normal fertility

Role of Ion Channels in the Sperm Acrosome Reaction

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